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Sex-specific Trans-regulatory Variation on the Drosophila melanogaster X Chromosome
University of Sheffield, Sheffield, United Kingdom; Department of Plant Ecology and Evolution, Uppsala University, Uppsala, Sweden.
Uppsala University, Uppsala, Sweden; Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.
Department of Animal Ecology, Uppsala University, Uppsala, Sweden; Department of Zoology, Stockholm University, Stockholm, Sweden.
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, The Institute of Technology. Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden.ORCID iD: 0000-0001-6112-9586
2015 (English)In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 11, no 2, 1-19 p., e1005015Article in journal (Refereed) Published
Abstract [en]

The X chromosome constitutes a unique genomic environment because it is present in onecopy in males, but two copies in females. This simple fact has motivated several theoreticalpredictions with respect to how standing genetic variation on the X chromosome should differfrom the autosomes. Unmasked expression of deleterious mutations in males and alower census size are expected to reduce variation, while allelic variants with sexually antagonisticeffects, and potentially those with a sex-specific effect, could accumulate on theX chromosome and contribute to increased genetic variation. In addition, incomplete dosagecompensation of the X chromosome could potentially dampen the male-specific effectsof random mutations, and promote the accumulation of X-linked alleles with sexually dimorphicphenotypic effects. Here we test both the amount and the type of genetic variation onthe X chromosome within a population of Drosophila melanogaster, by comparing the proportionof X linked and autosomal trans-regulatory SNPs with a sexually concordant anddiscordant effect on gene expression. We find that the X chromosome is depleted for SNPswith a sexually concordant effect, but hosts comparatively more SNPs with a sexually discordanteffect. Interestingly, the contrasting results for SNPs with sexually concordant anddiscordant effects are driven by SNPs with a larger influence on expression in females thanexpression in males. Furthermore, the distribution of these SNPs is shifted towards regionswhere dosage compensation is predicted to be less complete. These results suggest thatintrinsic properties of dosage compensation influence either the accumulation of differenttypes of trans-factors and/or their propensity to accumulate mutations. Our findings documenta potential mechanistic basis for sex-specific genetic variation, and identify the X as areservoir for sexually dimorphic phenotypic variation. These results have general implicationsfor X chromosome evolution, as well as the genetic basis of sex-specificevolutionary change.

Place, publisher, year, edition, pages
2015. Vol. 11, no 2, 1-19 p., e1005015
National Category
Evolutionary Biology
URN: urn:nbn:se:liu:diva-117546DOI: 10.1371/journal.pgen.1005015ISI: 000352081800062PubMedID: 25679222OAI: diva2:809451
Available from: 2015-05-04 Created: 2015-05-04 Last updated: 2015-06-02

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